F E Entomologie faunistique – Faunistic Entomology 2012 65, 49-68
Evidence of the role of predatory ants in natural
pest control in banana-sugarcane rotation systems
Jérôme Bailly Maitre
(1), Régis Goebel
(2)& Bernard Vercambre
(3)(1) European Topic Center on Biological Diversity, Muséum National d’Histoire Naturelle, 57 rue Cuvier, 75231 Paris Cedex 05, France. E-mail: [email protected]. Tél.: (+33) (0)1 40 79 38 68, Fax. (+33) (0)1 40 79 38 67. (2) CIRAD, Unité de Recherche Systèmes de culture annuels, Avenue Agropolis, F-34398 Montpellier Cedex 5,
France. E-mail: [email protected]
(3) CIRAD, Unité de Recherche Systèmes de culture annuels, Avenue Agropolis, F-34398 Montpellier Cedex 5, France. E-mail: [email protected]
Reçu le 1er septembre 2011, accepté le 13 février 2012
In Guadeloupe (French West Indies), sugarcane banana rotation is an alternative to intensive monoculture and increases vegetation diversity. Based on agroecology principles, this paper describes the structuration of the arthropod community at different stages of crop rotation with particular focus on two key pests: the banana weevil
Cosmopolites sordidus (Coleoptera: Curculionidae) and the pyralid moth of the genus Diatraea (Lepidoptera:
Pyralidae), known as stemborers. The functional inventory of the potential antagonists of these insect pests was mainly focused on ants which were the majority group collected in the trapping systems. The sugarcane agrosystem is less susceptible to attacks by pests than the banana agrosystem. In the context of crop rotation, sugarcane tends to limit infestation by the banana weevil to the first year of banana cropping, whereas banana does not help protect the sugarcane crop. Key information on targeted predators and their abundance and role in different agrosystems are given.
Keywords:vegetation diversity, arthropod community, Diatraea spp., Cosmopolites sordidus, antagonists.
Importance de la prédation par les fourmis en rotation canne/banane. En Guadeloupe, l’introduction de la
canne à sucre dans la monoculture de banane a contribué à une alternative aux agrosystèmes intensifs et favorise la diversité végétale. S’appuyant sur les principes de l’agroécologie, il a été étudié la structuration des groupes d’arthropodes à divers stades de la rotation culturale autour de deux bioagresseurs clés: le charançon du bananier
Cosmopolites sordidus (Coleoptera: Curculionidae) et les pyrales de la canne à sucre du genre Diatraea
(Lepidoptera: Pyralidae). L’inventaire fonctionnel des antagonistes potentiels de ces deux bioagresseurs établi au moyen de divers types de pièges se focalise dans cet article sur les fourmis qui occupent une part importante des captures. La canne à sucre est moins exposée aux attaques de la pyrale qui se situent en dessous du seuil de nuisibilité, alors que la bananeraie nécessite des traitements dès sa plantation. Dans le cadre de la rotation, la canne à sucre limite les infestations du charançon en première année de culture de la banane, alors que la banane ne favorise pas la protection de la canne. Ces résultats montrent qu’il est nécessaire d’approfondir les connaissances sur la prédation ciblée (pour les espèces à forte affinité avec la canne, dont le genre Solenopsis) dans un système banane-canne à sucre et les relations fonctionnelles entre les antagonistes identifiés.
Mots clés: diversité fonctionnelle, communauté d'arthropodes, Diatraea spp., Cosmopolites sordidus, antagonistes.
1. INTRODUCTION
Artificialization and biological simplification of intensive agrosystems such as monocultures could explain their vulnerability to pest infestation (Tilman et al., 2002).
In Guadeloupe (French West Indies), banana is traditionally grown as a monocrop with high levels of inputs (fertilizers, insecticides) to improve yield. In addition to degrading the soil
and causing progressive loss of soil biodiversity and chemical richness (Hulugalle et al., 1997), monocropping increases pest pressure and hence the use of pesticides to control them (Ganry, 2004). Monocropping thus has a negative impact on the environment including pollution of soils and phreatic groundwater systems, persistence of insecticides, one example being the persistence of chlordecone in Guadeloupe after many years of chemical treatments.
Growing sugarcane in rotation with banana in the Capesterre-Belle Eau region in Guadeloupe, led to a more diversified ecosystem as recommended by agroecology principles (Bianchi et al., 2006). Even though it is driven by economic considerations, this alternative to a monoculture has many advantages in terms of both agricultural practices (Risède, 2003) and environmental aspects (Ganry, 2004).
In the French West Indies, Jaffé et al. (1990) studied the predation of ants on the larvae of banana weevil Diaprepes abbreviatus L. Germar 1824 (Coleoptera: Curculionidae), but only in lime orchards. Sirjusinghi et al. (1992) published a global inventory of natural enemies (fungi, grubs, insects, vertebrates) of insect pests of sugarcane and banana in the West Indies.
These two crops are subject to high infestation by borer pests. The banana weevil Cosmopolites
sordidus, which is also a Curculionid, is a major
pest and causes serious damage to banana bulbs and pseudotrunks. If not controlled, this oligophagous pest can cause yields losses of up to 40 % (Ganry, 2004) and also reduce the plant life cycle. A detailed study of the biology and control strategies of this pest was made by Gold et al. (2001). The main insect pests of sugarcane in the West Indies are moth stemborers of the genus
Diatraea (Lepidoptera: Pyralidae) including two
species that are well known in South America,
Diatraea saccharalis Fabricius (1794) and Diatraea impersonatella Walker (1863) present in
Guadeloupe. Batches of eggs are laid on the top of sugarcane leaves and after hatching, the young larvae feed on green leaves for a week or so before penetrating the stalk to bore internodes and then leaving through an exit hole to pupate. Damage caused by borers leads to losses in terms of sugar yield and quality and cane biomass (Goebel & Way, 2009).
The banana-sugarcane rotation system has already been studied to compare the diversity of arthropod fauna at different growth periods of the rotation system (Caray, in lit.), the presence of fauna often being used as biological indicators (Duelli & Obrist, 1998; Missa et al., 2008). Caray (unpublished data) showed that arthropod diversity in the rotation system is lower than that observed in sugarcane monoculture. Another study by Vercambre (unpublished data) showed that after a banana crop, young sugarcane fields
were subject to increase the number of attacks during the first year followed by a decrease in pest infestation in the second year of cultivation. It was then hypothesized that the difference in infestation levels could be due to lack of predator diversity and thus of natural control. This is in line with the conclusions of Fuller & Reagan (1988), who pointed out that a reduction in predator abundance due to insecticide application in sugarcane and sorghum increased populations of moth borers and hence in the damage they cause.
The main aim of agricultural practices is not to favor biodiversity but to optimize it while increasing crop productivity. The aim of the present study was to identify and understand the functional component of the diversity of arthropod fauna and the role of predators in the natural control of two major pests D. saccharalis and
C. sordidus in banana-sugarcane rotation systems.
Particular attention was paid to the ant community (Formicidae), which is frequently used as a bioindicator of the level of diversity and environmental changes in the ecosystem, in comparison with other invertebrates (Lawton et
al., 1998; Underwood & Fisher, 2006). In fact the
Formicid family is the most commonly cited family in publications on the topic due to its diversity and functional importance (Mc Geoch, 2007) but also to its abundance in the ecosystem and to its ubiquity (Abera-Kalibata et al., 2007). Even though many studies mention the importance of these generalist predators in controlling pest populations (Symondson et al., 2002) particularly in agrosystems (Negm & Hensley, 1969; Roche & Abreu, 1983; Way & Khoo, 1992; Rossi & Fowler, 2000 & 2004), there is a paucity of information on the agricultural importance and role of ants in Guadeloupe, and their ability to maintain pest damage under economic thresholds.
2. MATERIAL AND METHODS 2.1. Experimental plots
Five agrosystems ("plots") representing different sugarcane-banana rotation systems were studied in the Capesterre-Belle-Eau region (16°09'53N 61°28'02W), Guadeloupe:
- CC: "Continuous" sugarcane cropping (Control 1), single-crop farming;
- BB: "Continuous" banana cropping (Control 2), single-crop farming;
- CB1: First year of banana after sugarcane (plantation);
- CB3: Third year of banana after sugarcane (2nd ratoon);
- BC1: First year of sugarcane after banana (plantation).
Another plot, BC3, (third year of sugarcane after banana) could have been tested; however as this situation is rare in Guadeloupe, it was decided not to include it in the experiment. Each plot had three replicates (Table 1). Hereafter all arthropods identified as predators and parasitoids of the banana weevil borer and of the sugarcane stemborer are referred to as antagonists.
2.2. Trapping systems
A method was implemented using ground and flight interception traps (data obtained from the aerial traps are informative), according to Duelli
et al. (1999) and taking into account the
conclusions of Missa et al. (2008). Traps used for data analysis
a/ Pitfall traps are open containers placed on the soil surface (can box type, height 157 mm, diameter 77 mm) in plastic cylindrical boxes for easy handling. The container is filled with a detergent solution (100 ml) to prevent insects from escaping and ensure their preservation. Each trap was removed at day 4 and day 7 to avoid additional water due to rainfall. Data were collated weekly and represent a sample unit. Pitfall traps are widely used to study insect fauna (Bestelmeyer et al., 2000).
b/ Sticky traps catch individuals present in the agrosystems. "Pelton type" sticky mesh green bands (BANDF-9917, Scotts France SAS; width 14 cm, including 12 cm of glued surface) were placed in the field at a height of 80 to 120 cm from the ground and attached to the banana tree trunks and to three sugarcane stalks in the same stool, in order to compare samples.
c/ In addition, two other sticky traps were used in the plots but the data were not used for statistical analysis. These were sticky yellow traps (height 334 mm, Adolive SARL) and/or double sticky face blue traps (dimensions 23x10 cm, Profertyl). These traps were attached to two sugarcane stalks or banana trunks 180 cm from the ground with 2 mm diameter nylon strings. Each plot had 5 trap locations and 2 types of trap were used at each location. The spacing is shown in Figure 1. Identification
Glue was removed from the trapped insects by immersing them in a petrol solution for 30 minutes. The insects were then preserved in vials filled with 70 % ethanol. Individuals bigger than 1 mm were identified under a microscope (x 50). Ants were identified using the Bolton classification (1994) and confirmed by a specialist in taxonomy of Formicidae.
Damage assessment in banana agrosystem The assessment technique was adapted from Vilardebo (1973). Samples of 60 banana bulbs were randomly chosen and dug up to a depth of 1-2 cm using a shovel. To avoid compromising the following harvest, the bulb should only be sampled on three-quarters of its periphery due to the presence of the young shoot in the last quarter.
5 4 3 2 1 2 3 4 5 1 Lenght: l Width: w l/6 w/2
Figure 1: Location of a trap in a plot. The spacing between sites is one sixth of the length of the plot.
The level of pest damage should be assessed soon after the harvest, as infestation by the weevil borer occurs on crop residues. The coefficient of infestation (CIb) shows the extent of damage to the banana stool (damage intensity index). The sum of the tunnels/boreholes found in the peripheral zone of the bulbs (from 0 to 100 %) shows the extent of damage in the study area: 5 (small boreholes), 20 (1/5 of the area infested), and then as the damage increases, 40, 60, 80, etc. According to Vilardebo (1973), different studies
have shown that infestation levels above 10 % often lead to significant yield losses.
Sampling for damage was conducted from June 23, 2008 to August 4, 2008. Fewer samples were collected from plot CB1 than from the other plots because this plot was harvested earlier by the grower.
Damage assessment in the sugarcane agrosystem The method used was the one described by Cochereau (1981). Each plot was divided into four
Figure 2: Importance of taxa (order and family) defined as antagonists with respect to all the antagonists trapped
in the banana (A) and sugarcane (B) systems. Data for CB3 are not presented here but did not strongly affect the results for banana. For instance, respectively in SB and PT, ants represent 19.19 % 5.38) and 64.58 % (+/-7.48) of all antagonists when CB3 data are excluded, and 21.90 % (+/-4.50) and 63.10 % (+/-6.67) when CB3 data are included. The standard error is included within the graph.
BB: "continuous" banana cropping (Control 2), single-crop farming; CB1: first year of banana after sugarcane (plantation); CB3: third year of banana after sugarcane (2nd ratoon); CC: "continuous" sugarcane cropping (Control 1), single-crop farming; BC1: first year of sugarcane after banana (plantation); banana (BB and CB1); sugarcane (CC and BC1); PT: catches in pitfall traps; SB: catches in sticky traps.
0 10 20 30 40 50 60 70 80 Tachinidae Reduviidae Hymenoptera (predator) Formicidae Forficulidae Coleoptera Blattelidae Aranea (%) PT SB 0 10 20 30 40 50 60 70 80 Tachinidae Reduviidae Hymenoptera (predator) Formicidae Forficulidae Coleoptera Blattelidae Aranea (%) PT SB
A
B
sub-plots of equal size, and then two sampling sites were randomly selected in each sub-plot. From a selected location, 25 consecutive stalks in the field (200 stalks per plot) were sampled and inspected for borer damage. Stalks were carefully checked for the presence of holes and damaged and undamaged internodes were counted starting from the bottom of the stalk.
All bored internodes were sliced with a knife and the damage intensity was rated on the basis of the size (length) of internal tunnels in the whole internode. A coefficient of infestation in sugarcane (CIc) is also used starting from 0 (no infestation) to 5 (serious internal damage with presence of external side shooting resulting from plant stress).
Field identification of the pest was based on the larvae and pupae collected. All samples were kept in the laboratory to check for parasitism. Similarly, all stages of parasitoids found were collected and kept for further identification. The level of pest damage to the two crops was determined not only on the basis of the percentage of infested plants (or stalks) but also on the intensity of infestation given by two indices CIb and CIc. Damage and pest sampling was conducted from June 9 to June 19, 2008, and a total of 1 200 stalks (20 622 internodes) were inspected.
Statistical analysis of data
The samples from each week were combined to obtain a pooled sample of fauna per trap for each sampling site. Due to the high variability of data collected, comparisons based on the fauna diversity between plots focused on the relative abundance (proportion) of taxa/individuals out of the whole catches. Instead of using statistical analysis comparing means, the Khi² test appeared to be the most relevant for this study whose aim was to highlight structural differences in the composition of the arthropod community.
For each plot/agrosystem, all damage assessment data were considered as non-parametric and were therefore subjected to non-parametric methods. The Kruskall-Wallis test was used to compare numbers while testing for the presence of a plot/treatment effect (= agrosystem). Independent means were also compared using the Wilcoxon Mann-Whitney test to test the extent of damage in relation with the agrosystem. A Khi² test was used
to compare qualitative data such as whether the plant was damaged or not.
3. RESULTS
No significant differences in monthly means of meteorological data were observed between the plots during the study period.
Global diversity and diversity within the antagonist community
All sugarcane plots were surveyed at the end of the crop cycle. Trap catches collected between June 10 and July 17, 2008 totaled 5 229 arthropods, representing 12 orders and 35 families (Table 2).
The following analyses focused on the comparison of the two crops to characterize three situations: sugarcane (CC and BC1); banana (BB and CB1); and CB3.
Importance of the trapping system
The classification of the individuals according to their functional activity in the agrosystem was adapted from different studies targeting arthropod families found to be generalist and/or specific predators of weevil borer and stem borer. Regarding global diversity, 21 families representing 1 675 individuals were considered active in the control of these pests (Table 2). The number of families (15) and the structure of the antagonist community were very similar in the two agrosystems. If plots CB3 are included, two new families, Ichneumonidae and Tenebrionidae, were added to the taxonomic richness previously observed in the banana agrosystem.
Both crops showed similar results in terms of insect catches due to the trap efficiency. The Formicidae family was strongly represented in pitfall trap catches (65 to 71 % depending on the agrosystem) while the sticky band traps caught a wider taxonomical range which was also more balanced in the number of catches. On the soil surface, the Coleoptera order was more frequently found in the banana than in sugarcane agrosystem, while the number of blattoptera (Blattaria) was higher in sugarcane. Forficula insects considered as predators were more frequently found in sticky traps in banana than in sugarcane as opposed to tachinid flies. The proportion of ants collected in sticky traps was higher in banana than in
sugarcane (p=0.034, Khi²=4.50), and results from CB3 confirmed this difference p<0.0001, Khi²=17.72). The difference was not significant on the surface of the soil (p=0.32, Khi²=0.98). Figure 2 shows the taxonomic distribution of the antagonists (orders and/or families) that had an impact on the pest population for each trap and each agrosystem.
Given their predominance in the traps, Formicidae were the subject of more detailed determination. Generalist in their predatory activities, these ants are abundant and ubiquistic whatever the disturbance level of the habitat surveyed. They have been particularly well studied in tropical environments, including agricultural habitats (Way & Khoo, 1992; Power, 1996).
The proportion of ants in the antagonist community varied depending on the agrosystem and the trap considered (Figure 3). On the soil surface (pitfall traps) ants were dominant, particularly in sugarcane. On the plants themselves (sticky traps) their number was lower. Comparisons within the same crop showed that the proportion of ants differed significantly only on sticky bands between BB-CB1 (p=0.0008, Khi²=11.09) and CC-BC1 (p=0.0014, Khi²=10.23). The same comparisons were not significant on the soil surface. Other analyses
between plots revealed differences between CC and BB both on the soil surface (p=0.033, Khi²=4.57) and in the vegetation (p=0.015, Khi²=5.95). In the banana crop, the proportion of ants in traps in CB3 differed significantly from that in BB both in pitfall traps (p=0.046, Khi²=3.98) and sticky traps (p<0.0001, Khi²=18.48).
Species inventory
The inventory of the 855 individuals collected (Table 3), which were distributed in four sub-families, 15 geniuses and 19 species, provided information on the distribution per plot (31.9 % in CC, 9.8 % in BC1, 9.2 % in BB, 21.0 % in CB1 and 28.1 % in CB3). Catches were biggest in the pitfall traps (80.9 %) and these also had the highest species richness (six more species than in the sticky traps). Most of the species were particularly mobile and were caught in different types of traps. Species Azteca sp.
(Dolichoderinae) and Pheidole sp1 (Myrmicinae) were only represented by reproductive (presence of wings) individuals which were not counted in this study.
In Guadeloupe, 59 species distributed in five sub-families species have already been described (Jaffé & Lattke, 1994). Our inventory added eight
0 20 40 60 80 100 BB CB3 CB1 BC1 CC (%) SB PT
Figure 3: Average proportion of ants per trapping system and agrosystem among all the arthropods trapped.
The standard error is included within the graph.
BB: "continuous" banana cropping (Control 2), single-crop farming; CB1: first year of banana after sugarcane (plantation); CB3: third year of banana after sugarcane (2nd ratoon); CC: "continuous" sugarcane cropping (Control 1), single-crop farming; BC1: first year of sugarcane after banana (plantation); PT: catches in pitfall traps; SB: catches in sticky traps.
new species to the previous lists: Nylanderia
pubens (Plate 1), Monomorium ebeninum (Plate
2), Solenopsis invicta (Plate 2), Pheidole vallifica (Plate 1), Cardiocondyla minutior, Cardiocondyla
obscurior (photo of the genus Cardiocondyla,
Plate 3), Hypoponera opaciceps, Odontomachus
brunneus (Plate 1).
The genus and species richness was higher in the sugarcane agrosystem than in banana including plots CB3. Only five species (S. invicta,
S. geminata (Plate 1), M. ebeninum, P. vallifica, T. bicarinatum) were found in both agrosystems
including N. pubens observed in the additional traps placed in banana (CB3 plots).
The sub-family Myrmicinae was most abundant and represented 76 % of the trap catches. The composition of the arthropod community differed in the two crops. Myrmicinae were more abundant in banana (100 % of the captures, and 95.6 % in CB3) than in sugarcane (45.5 %), which hosted Ponerinae and Dolichorinae families. Similarly, the genus Tetramorium represented 39.2 % and was particularly abundant in banana at 55.8 % of the catches (75.9 % in CB3) in comparison with sugarcane (2.4 %). At the species level, N. pubens was the most frequent species found in sugarcane (28.2 %) followed by E. ruidum (16.3 %, Plate 3). In banana, two ant species T. bicarinatum (49.1 %) and M. ebeninum (22.8 %) were very abundant in CB3 plots (respectively 69.5 % and 8.0 %). Although the species richness remained stable in banana (5-6 species), the structure of the ant community differed between the different plots.
Delabie et al. (2000) proposed an original method to group species: the notion of insect guilds that organizes taxons based on their role and biological preferences in the ecosystem. For example, guilds 1, 3, 7 and 8 (Delabie et al., 2000) are represented in our study. By grouping the generalist predators, true omnivores and omnivorous arboreal nesting dominants, guilds 7 and 8 include individuals that prospect on soil, litter and plant debris for feeding. At least 87.8 % of the individuals identified belonged to these guilds and species such as P.
pubens, M. ebeninum and T. bicarinatum totaled
71.7 %. Guilds 7 and 8 tended to be more widely represented in the sugarcane agrosystem (87.5 %) than in banana (83.9 % of all ants, and 92.4 % in CB3).
Damage assessment in the banana agrosystem Data on C. sordidus infestation are listed in Table 4. Damage levels differed significantly between the experimental plots in terms of the number of plants infested by the pest (df: 2, Khi²=91.69, p<0.0001) as well as the intensity of damage (df: 2, H=67.02, p<0.0001). In this sense, the comparisons 2x2 of plots BB-CB3 (Khi²=25.47), BB-CB1 (90.71) and CB3-CB1 (38.12) were all significant (df: 1, p<0.0001) in terms of the percentage of infested plants. The least damaged plots (in terms of the intensity of the infestation) were CB1 in comparison with plots BB and CB3 (p<0.0001 in the 2 cases) while plot BB tended to differ from plot CB3 (p=0.058).
Damage assessment in the sugarcane agrosystem Results are summarized in Table 5. The damage threshold was defined as 5 % of bored internodes. Despite a higher infestation of the plot (BC1), the level of infestation remained below this threshold. This result is not in agreement with previous work in the same region (in 2005) when BC1 plots had more than 5 % bored internodes while other CC plots had damage levels of between 0.1 and 1.3 %. The percentage of stalk damage differed significantly between both sugarcane agrosystems (df: 23, Khi²=147.5, p<0.0001), whereas the percentage of bored internodes (df: 23, Khi²= 18.13, p=0.75) and the intensity of the infestation CIc (z=-1.89, p=0.058) did not.
Both pest species were well established in the sugarcane single-crop system whereas
D. saccharalis appeared to be predominant in the
first year of sugarcane after banana.
4. DISCUSSION
The work presented here provides new key information on the importance of ant diversity in community of antagonists present in the banana-sugarcane rotation system. The study of arthropods (Duelli & Obrist 1998) using different trapping systems (Missa et al., 2008) is a common method to identify the arthropod diversity of agronomic interest, i.e. plays a functional role in insect control. Referring to the criteria listed by Missa et al. (2008) (cost, maintenance and easy setup, low impact on populations, etc.), the combination of pitfall traps and sticky traps was
particularly suitable for our study that focused on individuals moving in and around the plant, and that were assumed to be involved in the predation or parasitism of the targeted pest. The use of non-selective traps also allowed us to unravel the taxonomic diversity in the different agrosystems, species richness, and the presence of rare species in comparison with other trapping systems such as lure traps (Abera-Kalibata, 2007; Souza et al., 2010). The functional activity of the samples of insect collected, provided useful information on the composition of antagonist species which was more diversified in the vegetation than on the surface of the soil, and this was valid for both crops. For example, the catches revealed the importance of Formicidae.
These findings are in agreement with the results obtained by Underwood & Fisher (2006), who collected ants using different sampling methods and identified them as key factors for conservation purposes. In this regard, the taxonomy of ants is actually well advanced compared to other invertebrate groups (Matlock & Cruz, 2003). Even if statistical analyses were not always significant, many trends were highlighted in this study. On the soil surface, ants tend to be predominant when sugarcane is grown for several consecutive years (situations CC and CB1), as opposed to banana where their presence is lower, this result being similar to that observed when a new sugarcane plantation is established after banana (BC1). Known for its major role in different habitats (dominance and ecological abundance, eusocial behavior and diversified food regime) and its use in pest control programs (Hölldobler & Wilson, 1990; Way & Khoo, 1992), the Formicidae family is cited as efficient natural predators of weevil borers and pyralid moth borers. Our results underlined their affinity for the crop and their susceptibility to disturbances caused by crop rotation systems.
Many authors have pointed to the efficacy of ants in the suppression of C. sordidus (Gold et al., 2001; Abera-Kalibata et al., 2007) and stalk borers such as D. saccharalis and C. sacchariphagus, particularly at the egg stage and
first instar larva (Negm & Hensley, 1972; Adams
et al., 1981; Ali & Reagan, 1985; Goebel, 1999;
Rossi & Fowler, 2000).
For example, S. invicta, which are considered to be extremely voracious (Eubanks et al., 2002),
have been shown to play a major role in the control of borer populations, particularly in the USA (Negm & Hensley, 1969; Ali & Reagan, 1985). The species feeds on D. saccharalis eggs and larvae (Adams et al., 1981; Rossi & Fowler, 2000; Rossi & Fowler, 2004). In Guadeloupe, unlike the above mentioned results, S. invicta is not the predominant species in the sugarcane agrosystem. In this region, the species
W. auropunctata (Plate 2) is cited as a potential
natural enemy of C. sordidus while E. ruidum and
O. brunneus have been identified as active
predators of eggs and larvae of the sugarcane weevil borer D. abbreviatus (Sirjusinghi et al., 1992).
In our study, damage assessment revealed different levels of infestation. In the sugarcane fields surveyed, damage was below the economic injury level of 5 % internodes bored, indicating effective control of the sugarcane borer by its natural enemies, which was not the case for the banana weevil borer. Already shown in the first and second sugarcane ratoons (White,1980), this natural control intensifies when the sugarcane is grown for several consecutive years after banana, while the opposite effect is observed in the banana agrosystem. In the light of these observations, we can conclude that sugarcane is not favored by succeeding banana in the rotation system; the first year of sugarcane after banana (BC1) led to highest infestation levels compared to CC plots. Conversely, the banana crop appears to benefit from succeeding sugarcane, as is the case for nematodes (Risède, 2003) at least in the first year, as from the third year on, this benefit appears to decrease. Many observations suggest a major role of ants in pest regulation: abundance in the antagonist community at the ground level, mobility in and around the plants, the preference of Ponerinae and Dolichoderinae for sugarcane, observation of predation activities of the ant S.
invicta and their presence in the boreholes caused
by stemborers (Sirjusinghi et al., 1992; Rossi & Fowler, 2004).
These results will be confirmed by further experiments, particularly on the role and importance of ants and other predators such as the spiders in the control of populations of major pests. Other aspects such as intra and interspecific interactions (Sirjusinghi et al., 1992; Wing, 1983; Gillespie & Reimer, 1993) require additional investigation as does the agronomic interest of
agricultural pest even though its action has led to pesticide reduction (Long et al., 1987; Way & Khoo, 1992; Eubanks, 2001; Eubanks, 2002; Symondson et al., 2002).
Acknowledgements
Our thanks to the specialists who helped us identify the insect collection: J.-C. Ledoux, M. D. Marival (INRA) and G. Chovet, and to H.P. Aberlenc (CIRAD) for training in insect photography. We are grateful to J. Delabie for the identification of ant species and his very useful advice, as well as to B. Mac Sharry (ETC/BD-MNHN) for his expertise on GIS analysis.
This study also benefited from the logistic and scientific support of CIRAD staff in Guadeloupe: J.-C. Dagallier, J.-H. Daugrois and M. Dorel. Finally, we are very grateful to the growers F. Longueteau and L. Dormoy who allowed us access to their farms to conduct our experiments.
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Plates and tables
Plate 1: (from top to bottom): Odontomachus bruneus (Patton 1894) (Ponerinae): full-face and profile -
Nylanderia pubens (Forel 1893) (Formicinae): face and profile - Pheidole villifica (Formicinae):
face and profile - Solenopsis geminata (Fabricius 1804) (Myrmicinae): face and profile (scale: full-face 0.25 mm; profile 1 mm).
Plate 2: (from top to bottom): Solenopsis invicta (Buren 1972) (Myrmicinae): full-face and profile -
Monomorium ebeninum (Forel 1891) (Myrmicinae): full-face and profile - Wasmannia auropunctata
Plate 3: (from top to bottom): Camponotus sexguttatu (Fabricius 1793) (Formicinae): full-face and
profile - Cardiocondyla sp (Myrmicinae): face and profile - Cyphomyrmex sp (Myrmicinae): face and profile - Ectatomma ruidum (Roger 1860) (Ectatomminae): face and profile (scale: full-face 0.25 mm; profile 1 mm).
Table 1: Attributes of selected agrosystems Agrosystems (plots) Name of field (replicates) Area (ha)
Crop variety Planting
date
Geographical coordinates Average altitude (m)
BC1 Dinde5 1.77 B 69566 3.x.2007 16°00’59N 61°35’06W 47
BC1 Cressonniere3 1.63 B 69566 3.x.2007 16°01’12N 61°35’09W 64
BC1 Case à Nègre 1.21 B 69566 3.x.2007 16°01’25N 61°35’16W 86
CB3 Riz1 1.66 ZELIG + GAL 26.v.2005 16°01’25N 61°35’28W 95
CB3 Marquise1 1.26 GAL + JAFFA 23.vi.2005 16°01’39N 61°35’47W 139
CB3 Marquise2 1.26 JAFFA 23. vi .2005 16°01’36N 61°35’49W 138
BB Gaegaba2 1.68 Traditional 14.x.1999 16°01’41N 61°35’08W 98
BB Digue 3.08 Traditional 1.iii.2002 16°01’37N 61°35’27W 108
BB Monbin3 1.91 MA 13 + GAL 25. vi .2004 16°01’37N 61°35’39W 126 CB1 Helise2 1.18 MA 13 14. vi .2007 16°01’08N 61°35’21W 68 CB1 Helise3 1.30 MA 13 1. vi .2007 16°01’13N 61°35’25W 78 CB1 Helise4 0.87 MA 13 1. vi .2007 16°01’14N 61°35’23W 74 CC Solanne1 3.34 B 69566 2001 16°05’06N 61°34’12W 57 CC Solanne2 2.56 B 69566 2001 16°05’11N 61°34’11W 58 CC Anonyme 3.56 B 69566 2000 16°05’07N 61°33’59W 43
BB: "continuous" banana cropping (Control 2), single-crop farming; CB1: first year of banana after sugarcane (plantation); CB3: third year of banana after sugarcane (2nd ratoon); CC: "continuous" sugarcane cropping (Control 1), single-crop farming; BC1: first year of sugarcane after banana (plantation).
Table 2: Distribution of arthropods sampled in the banana-sugarcane rotation system according to order and family
Order Family BB CB3 CB1 BC1 CC Banana Sugarcane Pests targeted
Blattaria* Blattellidae* Karny 1908 x x x x x x x Sugarcane pest in Reunion Island (Goebel 1999)
Dermaptera* Forficulidae* Stephens 1829 x x x x x x x C. sordidus (Gold et al., 2001) and the sugarcane borer in
Reunion Island (Goebel, 1999)
Neuroptera Chrysopidae Schneider 1851 o o o x o x
Diptera* Tachinidae* o x x x x x
Three species introduced in the French West Indies between 1938 and 1954 (Astabie in lit.) to compete against the genus Diatraea:
Metagonistylum minense Townsend 1927, Lixophaga diatraeae
Townsend 1916 and Paratheresia claripalpis van der Wulp.
Conopidae x x x
Culicidae Meigen 1818 x x x x
Syrphidae o
Araneae* Lycosidae* Sundevall 1833 x x x o x o
Control of plant-eating insects and major actor in agrosystems (Cocquempot & Chambon, 1989), notably in sugarcane (Negm & Hensley, 1969). Omnivorous, they are mentioned as predators of the genus Diatraea (Negm & Hensley, 1972).
Tetragnathidae* Menge 1866 x x x x x x Anyphaenidae* Bertkau 1878 x x x x x x x Linyphiidae* Blackwall 1859 x x x x o x x Theridiidae* Sundevall 1833 o x x x x x x Salticidae* Blackwall 1841 x x x x x x x Oonopidae* Simon 1890 o x o x Araneidae* Clerck 1757 o o o
Hymenoptera* Formicidae* Latreille 1809 x x x x x x x More explanations below.
Sphecidae* Latreille 1802 o o Carnivorous larva feed on paralyzed insects carried to the nest by
adults (Roth, 1968).
Halictidae Thomson 1869 o o x x
Ichneumonidae* Latreille 1802 x o o Attacks mainly targeted on true and false caterpillars as well as
on Lepidoptera chrysalis (Roth, 1968).
Apidae Latreille 1802 o o o o
Vespidae* Latreille 1802 o o Feed on chewed larva (Roth, 1968).
Scoliidae Latreille 1802 o o
Coleoptera* Carabidae* Latreille 1802 x x x x x x x Natural enemy of C. sordidus (Gold et al., 2001) and D.
saccharalis (Negm & Hensley, 1972)
Anobiidae Fleming 1821 o o o o o o
Bostrichidae Latreille 1804 o o o
Elateridae Leach 1815 o o o
Scolytinae (Ipsidae) Latreille 1804 o x x o o x o
Order Family BB CB3 CB1 BC1 CC Banana Sugarcane Pests targeted
Coccinellidae Latreille 1807 o x o x x o x
Curculionidae* Latreille 1802 x x x o x x x C. sordidus (Gold et al., 2001)
Nitidulidae Latreille 1802 o o
Phytophagonidae x x x x x x x
Staphylinidae* Latreille 1802 x x x o x o C. sordidus (Gold et al., 2001)
Tenebrionidae* Latreille 1802 x x x x C. sordidus (Gold et al., 2001)
Hemiptera* Cercopidae Leach 1815 x x
Cicadellidae Latreille 1802 o o x o x
Coreidae Leach 1815 x x x o x o
Pentatomidae Leach 1815 x x x x x x
Reduviidae* Latreille 1807 x x x x x x x Natural enemy of C. sordidus (Sirjusinghi et al., 1992; Gold et
al., 2001).
Isoptera Termitidae Sands 1972 o x x x x x
Lepidoptera Undefined x x o x x x
Orthoptera Caelifera Ander 1936 x x x x x x x
Gryllidae Bolivar 1878 x x x x x x x
Tettigoniidae Krauss 1902 x x
Iulida Iulidae Leach 1814 x x x x x x x
Undefined Sp 1 x x x x x x x
Total Order/Family 12/36 10/22 11/28 10/25 11/24 10/23 11/28 12/29
*: families described in the literature as predators of one or both pests; x: informs on catches in pitfall traps (PT) and sticky traps (SB); o: species caught by a trapping system not used in this study.
BB: "continuous" banana cropping (Control 2), single-crop farming; CB1: first year of banana after sugarcane (plantation); CB3: third year of banana after sugarcane (2nd ratoon); CC: "continuous" sugarcane cropping (Control 1), single-crop farming; BC1: first year of sugarcane after banana (plantation); banana (BB and CB1); sugarcane (CC and BC1).
Table 3: Distribution of ants as a function of the agrosystem and crop, and their diet. Species Proportion (%) BB CB3 CB1 BC1 CC Banana Sugarca ne Trapping system Foraging
characteristics Involvement of the genus in pest control
Formicinae 13
Nylanderia pubens Forel 1893 12.4 o x x x x +PT / SB Omnivore
This genius was originally named Paratrechina.
An undefined species is attracted by C.
sordidus larvae (Abera-Kalibata et al.
2007).
Camponotus sexguttatus
Fabricius 1793 0.6 x +PT / SB Omnivore
Cited in the larval stage predation of the sugarcane weevil Diaprepes abbreviatus Linnaeus (1758) (Sirjusinghi et al. 1992)
Myrmicinae 76.1
Solenopsis geminata Fabricius
1804 5.8 x x x x x x PT Omnivore or
graminivore
Potentially involved in the control of C.
sordidus in Guadeloupe (Sirjusinghi et al.
1992) and D. saccharalis (Fowler et al. 1991)
Solenopsis invicta Buren 1972 3.4 x x x x x x +PT / SB
Brachymyrmex sp. 0.1 x x PT Omnivore
(nectarivore)
B. obscurior is mentioned as a predator of D. abbreviatus (Sirjusinghi et al. 1992)
Cyphomyrmex sp. 0.8 x x x +PT / SB
Monomorium ebeninum Forel
1891 15.1 x x x x x x x +PT / SB Omnivore
Wasmannia auropunctata
Roger 1863 2.7 x x x +PT / SB
Omnivore and nectarivore
Potential natural enemy of C. sordidus (Sirjusinghi et al. 1992)
Pheidole vallifica Forel 1901 7.7 x x x x x x x +PT / SB
Omnivore (maybe few graminivorous species)
Many species known as natural enemies of
C. sordidus (Sirjusinghi et al. 1992;
Abera-Kalibata et al. 2007) and D. saccharalis (Adams et al. 1981, Rossi & Fowler 2004), or of the African sugarcane borer Eldana
saccharina Walker in Africa (Girling
1978) and Chilo sacchariphagus Bojer in Reunion Island (Goebel 1999).
Pheidole sp1 - o x x PT / SB
Tetramorium undefined 3.8 x +PT / SB
Omnivore (nectarivore)
Predator of C. sordidus in Cuba (Roche & Abreu 1983) and in South America, de D.
abbreviatus in Florida (Sirjusinghi et al.
1992) and also of E. saccharina’s eggs (Girling 1978).
Tetramorium bicarinatum
Nylander 1846 35.4 x x x x x x +PT / SB
Species Proportion (%) BB CB3 CB1 BC1 CC Banana Sugarca ne Trapping system Foraging
characteristics Involvement of the genus in pest control
1899 than nectarivore abbreviatus in Porto Rico (Sirjusinghi et
al. 1992). Cardiocondyla obscurior
Wheeler, 1929 0.6 x x x PT
Ponerinae 8.7
Ectatomma ruidum Roger,
1860 6,8 x x x +PT / SB Generalist predator
This genus preys on arthropod eggs (Hölldobler & Wilson 1990) including eggs and larvae of D. abbreviatus (Sirjusinghi et al. 1992), and potentially D.
saccharalis (Rossi & Fowler 2004).
Odontomachus brunneus
Patton, 1894 1.7 x x PT Generalist predator
The species O. troglodytes is a predator of
C. sordidus eggs (Abera-Kalibata 2007)
and D. abbreviatus larvae (Sirjusinghi et
al. 1992)
Hypoponera opaciceps Mayr,
1887 0.2 x x PT
Generalist predator (mainly of micro-arthropods)
If a closed genus called Plectroctena Smith (1858) is described as an egg-parasite, the carnivorous genus Hypoponera seems to prefer springtails (Collembola) (Hölldobler & Wilson 1990).
Dolichoderinae 2.2
Tapinoma melanocephalum
Fabricius, 1793 2.2 x x SB Nectarivore
Genus described as predator of D.
abbreviatus (Sirjusinghi et al. 1992;
Abera-Kalibata et al. 2006).
Azteca sp
-
x x x x x +PT / SB Omnivore
Predator of weevils C. sordidus in banana and D. abbreviatus in sugarcane (Sirjusinghi et al. 1992)
Total (sub family/genus/species) 4/14/17 1/5/6 2/7/9 1/4/4 3/8/9 4/12/13 1/5/6 4/13/14
+: indicates the trap with the highest number of catches for the species; x: informs on catches in pitfall traps (PT) and sticky traps (SB); o: species caught by a trapping system not used in this study. The above statistics do not include flying individuals (Azteca sp and Pheidole sp1) or individuals caught by other trapping systems than pitfall traps and sticky traps. Statistics on the ‘banana’ agrosystem do not include data collected in the plot CB3. BB: "continuous" banana cropping (Control 2), single-crop farming; CB1: first year of banana after sugarcane (plantation); CB3: third year of banana after sugarcane (2nd ratoon); CC: "continuous" sugarcane cropping (Control 1), single-crop farming; BC1: first year of sugarcane after banana (plantation); banana (BB and CB1); sugarcane (CC and BC1).
Table 4: Summary of damage to banana agrosystem Name of field (replicates) Number of bulbs sampled Damaged plants (%) CIb M S-E Gaegaba2 60 83 17.25 2.27 Digue 60 88 24.33 3.01 Monbin3 60 58 9.00 1.50 Total BB 180 76.7 16.86 1.42 Riz1 60 25 2.42 0.68 Marquise1 60 58 15.08 2.85 Marquise2 60 70 21.58 3.49 Total CB3 180 51.1 13.03 1.62 Helise2 22 0 0 Helise3 15 0 0 Helise4 16 13 1.56 1.09 Total CB1 53 3.8 0.47 0.34
CIb: coefficient of Infestation assessed in banana crop; M: mean; S-E: standard-error. BB: "continuous" banana cropping (Control 2), single-crop farming; CB1: first year of banana after sugarcane (plantation); CB3: third year of banana after sugarcane (2nd ratoon).
Table 5: Main characteristics of damage and pest distribution in the sugarcane agrosystem.
Name of field (replicates) Damaged plants (%) Number of internodes Damaged internodes (%) CIc Diatraea (%)
M S-E M S-E M S-E M S-E D. s. D. i
Dinde5 13 3.68 338 7.38 1.87 0.59 0.027 0.01 83.3 16.7 Cressonniere3 15.5 1.92 351 7.10 1.8 0.27 0.026 0.006 50 50 Case à Nègre 45 5.79 375 5.78 6.8 1.37 0.113 0.024 91.7 8.3 Total BC1 24.5 3.78 355 4.93 3.48 0.69 0.055 0.012 85 15 Anonyme 22 4.66 549 5.29 1.32 0.29 0.021 0.005 100 0 Solanne 1 30 3.70 563 7.46 2.1 0.21 0.027 0.003 60 40 Solanne 2 18 3.93 401 24.09 1,6 0.33 0.027 0.005 50 50 Total CC 23.3 2.49 504 17.40 1.67 0.17 0.025 0.002 58.3 41.7
CIc: Rating of infestation in sugarcane; M: mean; S-E: standard error; D.s.: Diatraea sacharralis; D.i.: Diatraea
impersonatella. CC: "continuous" sugarcane cropping (Control 1), single-crop farming; BC1: first year of sugarcane
